Molecules and Cells

, Volume 35, Issue 5, pp 371–380 | Cite as

Phytochrome-interacting factors have both shared and distinct biological roles

  • Jinkil Jeong
  • Giltsu ChoiEmail author


Phytochromes are plant photoreceptors that perceive red and far-red light. Upon the perception of light in Arabidopsis, light-activated phytochromes enter the nucleus and act on a set of interacting proteins, modulating their activities and thereby altering the expression levels of ∼10% of the organism’s entire gene complement. Phytochromeinteracting factors (PIFs) belonging to Arabidopsis basic helix-loop-helix (bHLH) subgroup 15 are key interacting proteins that play negative roles in light responses. Their activities are post-translationally countered by light-activated phytochromes, which promote the degradation of PIFs and directly or indirectly inhibit their binding to DNA. The PIFs share a high degree of similarity, but examinations of pif single and multiple mutants have indicated that they have shared and distinct functions in various developmental and physiological processes. These are believed to stem from differences in both intrinsic protein properties and their gene expression patterns. In an effort to clarify the basis of these shared and distinct functions, we compared recently published genome-wide ChIP data, developmental gene expression maps, and responses to various stimuli for the various PIFs. Based on our observations, we propose that the biological roles of PIFs stem from their shared and distinct DNA binding targets and specific gene expression patterns.


bHLH transcription factor gene expression analysis light signaling phytochrome phytochrome-interacting factor 


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  1. Achard, P., Liao, L., Jiang, C., Desnos, T., Bartlett, J., Fu, X., and Harberd, N.P. (2007). DELLAs contribute to plant photomorphogenesis. Plant Physiol. 143, 1163–1172.PubMedCrossRefGoogle Scholar
  2. Al-Sady, B., Ni, W.M., Kircher, S., Schafer, E., and Quail, P.H. (2006). Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasorne-mediated degradation. Mol. Cell 23, 439–446.PubMedCrossRefGoogle Scholar
  3. Bae, G., and Choi, G. (2008). Decoding of light signals by plant phytochromes and their interacting proteins. Annu. Rev. Plant Biol. 59, 281–311.PubMedCrossRefGoogle Scholar
  4. Bu, Q., Zhu, L., and Huq, E. (2011). Multiple kinases promote light-induced degradation of PIF1. Plant Signal. Behav. 6, 1119–1121.PubMedCrossRefGoogle Scholar
  5. Casal, J.J. (2013). Photoreceptor signaling networks in plant responses to shade. Ann. Rev. Plant Biol. [Epub ahead of print]Google Scholar
  6. Casson, S.A., Franklin, K.A., Gray, J.E., Grierson, C.S., Whitelam, G.C., and Hetherington, A.M. (2009). phytochrome B and PIF4 regulate stomatal development in response to light quantity. Curr. Biol. 19, 229–234.PubMedCrossRefGoogle Scholar
  7. Chen, M., and Chory, J. (2011). Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21, 664–671.PubMedCrossRefGoogle Scholar
  8. Dash, S., Van Hemert, J., Hong, L., Wise, R.P., and Dickerson, J.A. (2012). PLEXdb: gene expression resources for plants and plant pathogens. Nucleic Acids Res. 40, D1194–1201.PubMedCrossRefGoogle Scholar
  9. Daviere, J.M., de Lucas, M., and Prat, S. (2008). Transcriptional factor interaction: a central step in DELLA function. Curr. Opin. Genet. Dev. 18, 295–303.PubMedCrossRefGoogle Scholar
  10. de Lucas, M., Daviere, J.M., Rodriguez-Falcon, M., Pontin, M., Iglesias-Pedraz, J.M., Lorrain, S., Fankhauser, C., Blazquez, M. A., Titarenko, E., and Prat, S. (2008). A molecular framework for light and gibberellin control of cell elongation. Nature 451, 480–U411.PubMedCrossRefGoogle Scholar
  11. Fairchild, C.D., Schumaker, M.A., and Quail, P.H. (2000). HFR1 encodes an atypical bHLH protein that acts in phytochrome A signal transduction. Genes Dev. 14, 2377–2391.PubMedGoogle Scholar
  12. Fankhauser, C., and Chory, J. (2000). RSF1, an Arabidopsis locus implicated in phytochrome A signaling. Plant Physiol. 124, 39–45.PubMedCrossRefGoogle Scholar
  13. Feng, S.H., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J.L., Wang, F., Chen, L.Y., Yu, L., Iglesias-Pedraz, J.M., Kircher, S., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451, 475–U479.PubMedCrossRefGoogle Scholar
  14. Filichkin, S.A., Breton, G., Priest, H.D., Dharmawardhana, P., Jaiswal, P., Fox, S.E., Michael, T.P., Chory, J., Kay, S.A., and Mockler, T.C. (2011). Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cisregulatory modules. PLoS One 6, e16907.PubMedCrossRefGoogle Scholar
  15. Franklin, K.A., Lee, S.H., Patel, D., Kumar, S.V., Spartz, A.K., Gu, C., Ye, S.Q., Yu, P., Breen, G., Cohen, J.D., et al. (2011). PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc. Natl. Acad. Sci. USA 108, 20231–20235.PubMedCrossRefGoogle Scholar
  16. Groszmann, M., Paicu, T., Alvarez, J.P., Swain, S.M., and Smyth, D.R. (2011). SPATULA and ALCATRAZ, are partially redundant, functionally diverging bHLH genes required for Arabidopsis gynoecium and fruit development. Plant J. 68, 816–829.PubMedCrossRefGoogle Scholar
  17. Hartweck, L.M. (2008). Gibberellin signaling. Planta 229, 1–13.PubMedCrossRefGoogle Scholar
  18. Heisler, M.G., Atkinson, A., Bylstra, Y.H., Walsh, R., and Smyth, D. R. (2001). SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 128, 1089–1098.PubMedGoogle Scholar
  19. Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O., and Fankhauser, C. (2009). Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 28, 3893–3902.PubMedCrossRefGoogle Scholar
  20. Hornitschek, P., Kohnen, M.V., Lorrain, S., Rougemont, J., Ljung, K., Lopez-Vidriero, I., Franco-Zorrilla, J.M., Solano, R., Trevisan, M., Pradervand, S., et al. (2012). Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J. 71, 699–711.PubMedCrossRefGoogle Scholar
  21. Huq, E., and Quail, P.H. (2002). PIF4, a phytochrome-interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis. EMBO J. 21, 2441–2450.PubMedCrossRefGoogle Scholar
  22. Huq, E., Al-Sady, B., Hudson, M., Kim, C.H., Apel, M., and Quail, P.H. (2004). PHYTOCHROME-INTERACTING FACTOR 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305, 1937–1941.PubMedCrossRefGoogle Scholar
  23. Kami, C., Lorrain, S., Hornitschek, P., and Fankhauser, C. (2010). Light-regulated plant growth and development. Curr. Top. Dev. Biol. 91, 29–66.PubMedCrossRefGoogle Scholar
  24. Kidokoro, S., Maruyama, K., Nakashima, K., Imura, Y., Narusaka, Y., Shinwari, Z.K., Osakabe, Y., Fujita, Y., Mizoi, J., Shinozaki, K., et al. (2009). The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol. 151, 2046–2057.PubMedCrossRefGoogle Scholar
  25. Kim, J., Yi, H., Choi, G., Shin, B., Song, P.S., and Choi, G. (2003). Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15, 2399–2407.PubMedCrossRefGoogle Scholar
  26. Koini, M.A., Alvey, L., Allen, T., Tilley, C.A., Harberd, N.P., Whitelam, G.C., and Franklin, K.A. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr. Biol. 19, 408–413.PubMedCrossRefGoogle Scholar
  27. Kumar, S.V., Lucyshyn, D., Jaeger, K.E., Alos, E., Alvey, E., Harberd, N.P., and Wigge, P.A. (2012). Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484, 242–245.PubMedCrossRefGoogle Scholar
  28. Laubinger, S., Zeller, G., Henz, S.R., Sachsenberg, T., Widmer, C.K., Naouar, N., Vuylsteke, M., Scholkopf, B., Ratsch, G., and Weigel, D. (2008). At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana. Genome Biol. 9, R112.PubMedCrossRefGoogle Scholar
  29. Lee, C.M., and Thomashow, M.F. (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 109, 15054–15059.PubMedCrossRefGoogle Scholar
  30. Leivar, P., and Quail, P.H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16, 19–28.PubMedCrossRefGoogle Scholar
  31. Leivar, P., Monte, E., Oka, Y., Liu, T., Carle, C., Castillon, A., Huq, E., and Quail, P.H. (2008a). Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photo-morphogenesis in darkness. Curr. Biol. 18, 1815–1823.PubMedCrossRefGoogle Scholar
  32. Leivar, P., Monte, E., Al-Sady, B., Carle, C., Storer, A., Alonso, J.M., Ecker, J.R., and Quail, P.H. (2008b). The Arabidopsis phytochrome-interacting factor PIF7, together with PIF3 and PIF4, regulates responses to prolonged red light by modulating phyB levels. Plant Cell 20, 337–352.PubMedCrossRefGoogle Scholar
  33. Leivar, P., Tepperman, J.M., Monte, E., Calderon, R.H., Liu, T.L., and Quail, P.H. (2009). Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21, 3535–3553.PubMedCrossRefGoogle Scholar
  34. Leivar, P., Tepperman, J.M., Cohn, M.M., Monte, E., Al-Sady, B., Erickson, E., and Quail, P.H. (2012). Dynamic antagonism between phytochromes and PIF family basic helix-loop-helix factors induces selective reciprocal responses to light and shade in a rapidly responsive transcriptional network in Arabidopsis. Plant Cell 24, 1398–1419.PubMedCrossRefGoogle Scholar
  35. Li, J., Li, G., Wang, H., and Wang Deng, X. (2011). Phytochrome signaling mechanisms. Arabidopsis Book 9, e0148.PubMedGoogle Scholar
  36. Li, L., Peng, W., Liu, Q., Zhou, J., Liang, W., and Xie, X. (2012a). Expression Patterns of OsPIL11, a Phytochrome-interacting factor in rice, and preliminary analysis of its roles in light signal transduction. Rice Sci. 19, 263–268.CrossRefGoogle Scholar
  37. Li, L., Ljung, K., Breton, G., Schmitz, R.J., Pruneda-Paz, J., Cowing-Zitron, C., Cole, B.J., Ivans, L.J., Pedmale, U.V., Jung, H.S., et al. (2012b). Linking photoreceptor excitation to changes in plant architecture. Genes Dev. 26, 785–790.PubMedCrossRefGoogle Scholar
  38. Lorrain, S., Allen, T., Duek, P.D., Whitelam, G.C., and Fankhauser, C. (2008). Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J. 53, 312–323.PubMedCrossRefGoogle Scholar
  39. Lorrain, S., Trevisan, M., Pradervand, S., and Fankhauser, C. (2009). Phytochrome interacting factors 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J. 60, 449–461.PubMedCrossRefGoogle Scholar
  40. Maere, S., Heymans, K., and Kuiper, M. (2005). BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21, 3448–3449.PubMedCrossRefGoogle Scholar
  41. Makkena, S., and Lamb, R.S. (2013). The bHLH transcription factor SPATULA regulates root growth by controlling the size of the root meristem. BMC Plant Biol. 13, 1.PubMedCrossRefGoogle Scholar
  42. Matsushita, T., Mochizuki, N., and Nagatani, A. (2003). Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 424, 571–574.PubMedCrossRefGoogle Scholar
  43. Mockler, T.C., Michael, T.P., Priest, H.D., Shen, R., Sullivan, C.M., Givan, S.A., McEntee, C., Kay, S.A., and Chory, J. (2007). The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb. Symp. Quant. Biol. 72, 353–363.PubMedCrossRefGoogle Scholar
  44. Nakamura, Y., Kato, T., Yamashino, T., Murakami, M., and Mizuno, T. (2007). Characterization of a set of phytochrome-interacting factor-like bHLH proteins in Oryza sativa. Biosci. Biotechnol. Biochem. 71, 1183–1191.PubMedCrossRefGoogle Scholar
  45. Ni, M., Tepperman, J.M., and Quail, P.H. (1998). PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95, 657–667.PubMedCrossRefGoogle Scholar
  46. Nozue, K., Covington, M.F., Duek, P.D., Lorrain, S., Fankhauser, C., Harmer, S.L., and Maloof, J.N. (2007). Rhythmic growth explained by coincidence between internal and external cues. Nature 448, 358–361.PubMedCrossRefGoogle Scholar
  47. Oh, E., Kim, J., Park, E., Kim, J.I., Kang, C., and Choi, G. (2004). PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16, 3045–3058.PubMedCrossRefGoogle Scholar
  48. Oh, E., Yamaguchi, S., Kamiya, Y., Bae, G., Chung, W.I., and Choi, G. (2006). Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J. 47, 124–139.PubMedCrossRefGoogle Scholar
  49. Oh, E., Kang, H., Yamaguchi, S., Park, J., Lee, D., Kamiya, Y., and Choi, G. (2009). Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis. Plant Cell 21, 403–419.PubMedCrossRefGoogle Scholar
  50. Oh, E., Zhu, J.Y., and Wang, Z.Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802–U864.PubMedCrossRefGoogle Scholar
  51. Oka, Y., Matsushita, T., Mochizuki, N., Suzuki, T., Tokutomi, S., and Nagatani, A. (2004). Functional analysis of a 450-amino acid Nterminal fragment of phytochrome B in Arabidopsis. Plant Cell 16, 2104–2116.PubMedCrossRefGoogle Scholar
  52. Park, E., Kim, J., Lee, Y., Shin, J., Oh, E., Chung, W.I., Liu, J.R., and Choi, G. (2004). Degradation of phytochrome interacting factor 3 in phytochrome-mediated light signaling. Plant Cell Physiol. 45, 968–975.PubMedCrossRefGoogle Scholar
  53. Park, E., Park, J., Kim, J., Nagatani, A., Lagarias, J.C., and Choi, G. (2012). Phytochrome B inhibits binding of phytochrome-interacting factors to their target promoters. Plant J. 72, 537–546.PubMedCrossRefGoogle Scholar
  54. Penfield, S., Josse, E.M., Kannangara, R., Gilday, A.D., Halliday, K.J., and Graham, I.A. (2005). Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr. Biol. 15, 1998–2006.PubMedCrossRefGoogle Scholar
  55. Penfield, S., Josse, E.M., and Halliday, K.J. (2010). A role for an alternative splice variant of PIF6 in the control of Arabidopsis primary seed dormancy. Plant Mol. Biol. 73, 89–95.PubMedCrossRefGoogle Scholar
  56. Rajani, S., and Sundaresan, V. (2001). The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr. Biol. 11, 1914–1922.PubMedCrossRefGoogle Scholar
  57. Salter, M.G., Franklin, K.A., and Whitelam, G.C. (2003). Gating of the rapid shade-avoidance response by the circadian clock in plants. Nature 426, 680–683.PubMedCrossRefGoogle Scholar
  58. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Scholkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37, 501–506.PubMedCrossRefGoogle Scholar
  59. Sessa, G., Carabelli, M., Sassi, M., Ciolfi, A., Possenti, M., Mittempergher, F., Becker, J., Morelli, G., and Ruberti, I. (2005). A dynamic balance between gene activation and repression regulates the shade avoidance response in Arabidopsis. Genes Dev. 19, 2811–2815.PubMedCrossRefGoogle Scholar
  60. Shen, H., Moon, J., and Huq, E. (2005). PIF1 is regulated by lightmediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J. 44, 1023–1035.PubMedCrossRefGoogle Scholar
  61. Shen, Y., Khanna, R., Carle, C.M., and Quail, P.H. (2007). Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiol. 145, 1043–1051.PubMedCrossRefGoogle Scholar
  62. Shin, J., Kim, K., Kang, H., Zulfugarov, I.S., Bae, G., Lee, C.H., Lee, D., and Choi, G. (2009). Phytochromes promote seedling light responses by inhibiting four negatively-acting phytochrome-interacting factors. Proc. Natl. Acad. Sci. USA 106, 7660–7665.PubMedCrossRefGoogle Scholar
  63. Soh, M.S., Kim, Y.M., Han, S.J., and Song, P.S. (2000). REP1, a basic helix-loop-helix protein, is required for a branch pathway of phytochrome A signaling in Arabidopsis. Plant Cell 12, 2061–2074.PubMedGoogle Scholar
  64. Stephenson, P.G., Fankhauser, C., and Terry, M.J. (2009). PIF3 is a repressor of chloroplast development. Proc. Natl. Acad. Sci. USA 106, 7654–7659.PubMedCrossRefGoogle Scholar
  65. Todaka, D., Nakashima, K., Maruyama, K., Kidokoro, S., Osakabe, Y., Ito, Y., Matsukura, S., Fujita, Y., Yoshiwara, K., Ohme-Takagi, M., et al. (2012). Rice phytochrome-interacting factor-like protein OsPIL1 functions as a key regulator of internode elongation and induces a morphological response to drought stress. Proc. Natl. Acad. Sci. USA 109, 15947–15952.PubMedCrossRefGoogle Scholar
  66. Toledo-Ortiz, G., Huq, E., and Quail, P.H. (2003). The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15, 1749–1770.PubMedCrossRefGoogle Scholar
  67. Yamashino, T., Matsushika, A., Fujimori, T., Sato, S., Kato, T., Tabata, S., and Mizuno, T. (2003). A link between circadian-controlled bHLH factors and the APRR1/TOC1 quintet in Arabidopsis thaliana. Plant Cell Physiol. 44, 619–629.PubMedCrossRefGoogle Scholar
  68. Yang, H.Q., Tang, R.H., and Cashmore, A.R. (2001). The signaling mechanism of Arabidopsis CRY1 involves direct interaction with COP1. Plant Cell 13, 2573–2587.PubMedGoogle Scholar
  69. Yang, J., Lin, R., Sullivan, J., Hoecker, U., Liu, B., Xu, L., Deng, X.W., and Wang, H. (2005). Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17, 804–821.PubMedCrossRefGoogle Scholar
  70. Zeller, G., Henz, S.R., Widmer, C.K., Sachsenberg, T., Ratsch, G., Weigel, D., and Laubinger, S. (2009). Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using wholegenome tiling arrays. Plant J. 58, 1068–1082.PubMedCrossRefGoogle Scholar
  71. Zhang, Y., Mayba, O., Pfeiffer, A., Shi, H., Tepperman, J.M., Speed, T.P., and Quail, P.H. (2013). A quartet of PIF bHLH factors provides a transcriptionally centered signaling hub that regulates seedling morphogenesis through differential expression-patterning of shared target genes in Arabidopsis. PLoS Genet. 9, e1003244.PubMedCrossRefGoogle Scholar
  72. Zhong, S., Shi, H., Xue, C., Wang, L., Xi, Y., Li, J., Quail, P.H., Deng, X.W., and Guo, H. (2012). A molecular framework of light-controlled phytohormone action in Arabidopsis. Curr. Biol. 22, 1530–1535.PubMedCrossRefGoogle Scholar

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© The Korean Society for Molecular and Cellular Biology and Springer Netherlands 2013

Authors and Affiliations

  1. 1.Department of Biological SciencesKorea Advanced Institute of Science and TechnologyDaejeonKorea

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